Stable epigenetic effects impact adaptation in allopolyploid orchids (Dactylorhiza: Orchidaceae)

Abstract

Epigenetic information includes heritable signals that modulate gene expression but are not encoded in the primary nucleotide sequence. We have studied natural epigenetic variation in three allotetraploid sibling orchid species (Dactylorhiza majalis s.str, D. traunsteineri s.l., and D. ebudensis) that differ radically in geography/ecology. The epigenetic variation released by genome doubling has been restructured in species-specific patterns that reflect their recent evolutionary history and have an impact on their ecology and evolution, hundreds of generations after their formation. Using two contrasting approaches that yielded largely congruent results, epigenome scans pinpointed epiloci under divergent selection that correlate with eco-environmental variables, mainly related to water availability and temperature. The stable epigenetic divergence in this group is largely responsible for persistent ecological differences, which then set the stage for species-specific genetic patterns to accumulate in response to further selection and/or drift. Our results strongly suggest a need to expand our current evolutionary framework to encompass a complementary epigenetic dimension when seeking to understand population processes that drive phenotypic evolution and adaptation.

FIG. 1.

Epigenetic patterns in sibling polyploid Dactylorhiza. (A) The allotetraploid Dactylorhiza traunsteineri at a natural site in Yorkshire, England. (B) PCoA (goodness of fit 0.87 at P = 0.001) of methylation status of allotetraploids D. majalis s. str. (blue symbols), D. traunsteineri s.l. (dark purple symbols), and D. ebudensis (pink symbols). Geographical provenance is indicated by symbol shapes: squares, Pyrenees; diamonds, Britain; triangles, Scandinavia; circles, Alps. The dotted line encloses samples from Yorkshire, England, and the dashed line D. traunsteineri s.l. samples from northwestern Scotland.

FIG. 2.

Loci under selection as indicated by SAM (Joost et al. 2007). (A–N) Graphs of the logistic sigmoid functions, symbolized with lines, corresponding to relevant pairs of epigenetic markers and their most significantly associated environmental variable (table 1). Symbols indicate the observed within-population frequency of the given marker for the corresponding value of the investigated ecoclimatic parameter. The shape and color of the symbols follow figure 1. (O) Histogram showing the environmental variables that significantly explain patterns of alternative epialleles. Some methylation markers are associated with more than one ecological variable (table 1).

FIG. 3.

Scan for epiloci under selection performed using BayeScan (Foll and Gaggiotti 2008). The PP for a locus to be under natural selection is shown on a log scale on the x axis (see also table 1). The open symbols indicate adaptive markers indentified with SAM. The three arrows on the x axis from left to right show the minimum threshold for strong, very strong, and decisive evidence for selection on Jeffrey’s scale (Foll and Gaggiotti 2008). Note that for epilocus b5, log¹⁰(BF) = 1,000, but the program places it in the graph at the value 5 because of space limitations.